Research, 2014 Vol. 29, No. 3, 229–236, http://dx.doi.org/10.1080/0269249X.2014.889041

The Didymo story: the role of low dissolved phosphorus in the formation of Didymosphenia geminata blooms MAX L. BOTHWELL1∗, BRAD W. TAYLOR2,3 & CATHY KILROY4 1Environment Canada, Pacific Biological Station, Nanaimo, , Canada 2Dept of Biological Sciences, Dartmouth College, Hanover, , USA 3Rocky Mountain Biological Laboratory, Crested Butte, , USA 4National Institute of Water and Atmospheric Research Ltd., Christchurch, New Zealand

We outline, in chronological sequence, the events and findings over 25 years that have shaped our understanding of Didymosphenia geminata (Lyngbye) M. Schmidt blooms. Starting with the first appearance of D. geminata mats in streams on Vancouver Island in the late 1980s and followed years later by blooms in Iceland, and Poland, D. geminata blooms were enigmatic for nearly 20 years. Early papers exploring whether blooms were caused by environmental change consistently failed to identify any specific factor(s) associated with their onset. Following the D. geminata outbreak in New Zealand in 2004 that seemed to result from an introduction of the species, the possibility that blooms that had previously occurred elsewhere in the world might also be explained by the introduction and movement among watersheds of a new variant with a bloom-forming tendency was touted and widely accepted. Now, however, the identification of very low soluble reactive phosphorus (SRP; below ∼2 ppb) as the proximate cause of bloom formation, has led to the more likely explanation that D. geminata blooms are the result of large-scale human intervention in climatic, atmospheric and edaphic processes that favour this ultra-oligotrophic species. In this new view, blooms of D. geminata are not simply due to the introduction of cells into new areas. Rather, bloom formation occurs when the SRP concentration is low, or is reduced to low levels by the process of oligotrophication. Mechanisms that potentially cause oligotrophication on global and regional scales are identified. Keywords: river diatom blooms, rock snot, Didymo, phosphorus limitation, global change, atmospheric N-deposition, N-enrichment of landscapes, dissolved phosphorus

The early years (1988–1998) of D. geminata-affected rivers on Vancouver Island were Modern episodes of Didymosphenia geminata (Lyngbye) taken during site visits (Fig. 1) and included on an M. Schmidt blooms in rivers were first systematically doc- early website describing the blooms (http://www.env.gov. umented on Vancouver Island, British Columbia in the late bc.ca/wat/wq/didy_bcstrms.html). 1980s (Sherbot & Bothwell 1993, Bothwell et al. 2009). Didymosphenia geminata is native to British Columbia, British Columbia Ministry of Environment (BCMoE) offi- as established by some of the earliest published records cials conducting routine water-quality monitoring in rivers of this species (Lord 1866, Cleve 1894–1896). Because downstream of municipalities in 1988 noticed patchy accu- D. geminata was a native species, a pressing question in the mulations of slimy looking material covering rocks in the 1980s was whether the blooms on Vancouver Island were Heber River, upstream of the town of Gold River. One year new events, or simply newly reported. Because the dense later, several kilometres of the Heber River were covered in benthic mats were occurring in more remote, sparsely pop-

Downloaded by [ Fish and Wildlife] at 10:39 18 December 2014 heavy mats. Microscopic examination of the mats revealed ulated areas of the island, this was not an easy question to the stalk-producing diatom D. geminata. The appearance address. Personal testimonies and scientific grey literature of thick algal mats was unusual because the Heber River, were evaluated. For example, mute evidence was avail- like most rivers on Vancouver Island, is nutrient-poor and able in the writings of Roderick Haig-Brown (1908–1976) extensive algal accumulations upstream of known human (Fig. 2). Widely recognized as the 20th century’s finest and nutrient inputs were unprecedented. most prolific angler writer, Haig-Brown lived on Vancou- In 1993, an ad hoc group of biologists and chemists ver Island most of his adult life and was a pioneering river (M. Clark, R. Nordin, J. Deniseger, L. Erikson and C. conservationist. He fished Vancouver Island’s rivers and Wightman) from the BCMoE was established to exam- wrote about them for four decades. In Fisherman’s Fall ine the blooms and determine their causes. Photographs Haig-Brown (1964) describes two of his favourite rivers,

∗Corresponding author. E-mail: [email protected] (Received 5 September 2013; accepted 20 January 2014)

© 2014 Copyright of the Crown in Canada. Published by Taylor & Francis. This is an Open Access article. Non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly attributed, cited, and is not altered, transformed, or built upon in any way, is permitted. The moral rights of the named author(s) have been asserted. 230 Bothwell et al.

Fig. 2. Roderick Haig-Brown (1908–1976). A pioneer river conservationist, prolific author and resident fly fisherman of Van- couver Island for 42 years. No mention of nuisance benthic algal mats occurs in his writings. (Reproduced with permission of the Haig-Brown Institute.) Fig. 1. The British Columbia Didymosphenia ad hoc group viewing the D. geminata bloom in the Englishman River in 1993.

In the late 1970s, Fisheries and Oceans Canada con- ducted a study of the impact of nutrients discharged by the Heber and the Stamp, in both of which D. geminata fish hatcheries into rivers in British Columbia by quanti- blooms were documented in the 1990s. If these blooms had fying algal biomass and diatom species abundance (Munro occurred in his lifetime, Haig-Brown would most likely et al. 1985). The Puntledge River on Vancouver Island was have seen them and written about them, but no mention included in this study. Between 1978 and 1980, D. geminata appears in his works. was never sufficiently abundant to make the list of quan- The weakness of Haig-Brown’s testimony is that tifiable diatom taxa, although it was occasionally present Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 absence of evidence is not evidence of absence. For this (Munro et al. 1985). Starting in 1991 and continuing to reason, confirmation from long-time observers of Vancou- the present, D. geminata accumulations persist in varying ver Island rivers was sought. In 1976, the Fish and Wildlife degrees in the Puntledge River. Munro et al. (1985) cor- Branch of BCMoE engaged a team of professional fish- roborate that D. geminata was present in Vancouver Island eries biologists as a Steelhead Snorkel Survey Team (SSST) rivers prior to 1989, but in low abundance. to conduct annual censuses of steelhead escapement in The most likely factors for increased benthic in response to diminishing returns to Vancouver Island rivers. streams are typically either eutrophication (i.e., increased For 13 years, the SSST annually snorkel-surveyed the cali- concentration of nutrients, most often phosphorus) or brated reaches of many rivers and filed reports on steelhead declines in the intensity of physical disturbance or scour numbers. Starting in the early 1990s, the team noted that (Biggs & Close 1989, Biggs 2000). In 1993, we exam- benthic surfaces were being covered with thick brown ined water chemistry (BCMoE Environmental Monitoring mucilaginous mats that had not occurred in the preceding System Web Reporting) and hydrological (Water Survey of decade (L. Carswell, G. Horncastle, R. Hooton, R. Axford Canada, HYDAT 1992) databases for rivers on Vancouver and S. Hay, pers. commun.). Notes from the SSST helped Island. Although the analysis was hampered by a 3 ppb min- document the development of D. geminata proliferations imum detection limit for SRP, there was no indication that among rivers on Vancouver Island. the onset of blooms resulted from either an increase in SRP The Didymo story 231

or benign hydrological conditions (Sherbot & Bothwell exists (James et al. 2013). Although greater solar exposure 1993). can increase D. geminata stalk length (Kilroy & Bothwell In the 1990s, ground level increases in solar ultraviolet 2011a) and has been associated with greater bloom devel- radiation (UVR) resulting from global ozone depletion were opment (James et al. 2013), it appears that the UVR portion identified as a potential threat to aquatic ecosystems at mid of the solar spectrum does not play a major role in D. gemi- and higher latitudes (Häder & Worrest 1991). Unshaded, nata blooms (Kilroy & Bothwell 2011b, Kilroy & Bothwell shallow, clear water streams were especially vulnerable 2014). (Bothwell et al. 1994). Although the inhibition of attached The net result of investigating D. geminata blooms on riverine diatom communities by natural UVR was signifi- Vancouver Island in the early years was that, although cant, of most relevance was the finding that some species it was a native species, the blooms appeared to be a of stalked in the genera Gomphoneis and Cymbella new phenomenon, and there was no obvious change in appeared to be preferentially favoured under exposure to environmental conditions that might explain them. UV light (Bothwell et al. 1993). Didymosphenia geminata, however, was not found in the experiment. A later, in situ, experiment was run in 1995 to assess On the boots of fishermen the deleterious effects of UVR on aquatic insects (Kelly The onset of D. geminata blooms in New Zealand in 2004 2001). During a 70-day experiment, diatom samples were was widely attributed to the incursion of a new species collected and enumerated, but at the time, the data were (Kilroy 2004). This suggestion reignited questions about not analysed. We recently analysed the Kelly data. Two- the cause of blooms on Vancouver Island 15 years previ- way analysis of variance (ANOVA) revealed no consistent ously. Was the explanation for blooms that resulted from an effect of solar UVR on the abundance of D. geminata over introduction in New Zealand also applicable to Vancouver a 70-day period relative to other diatom taxa (p = 0.71) Island? Didymosphenia geminata was a native species in (Fig. 3). Although a positive relationship would have pro- British Columbia, but could a new bloom-forming variant vided a plausible explanation for D. geminata blooms, the have been introduced in the 1990s? Might this be the rea- data do not support this conclusion. son we had been unable to make sense of the blooms in the More recent research in New Zealand demonstrated an northern hemisphere? initial, inhibitory effect of UVR on D. geminata cell divi- On Vancouver Island, the British Columbia Steelhead sion that diminished after six days (Kilroy & Bothwell Harvest Questionnaire database was used to quantify angler 2011b). Stalk lengths are also often reduced under exposure activity on selected rivers between 1968 and 2003 and to UVR (Kilroy and Bothwell 2014). No positive rela- revealed a three- to fourfold increase in angler days on tionship between UVR and D. geminata growth has been some rivers in the mid-1980s leading up to the D. geminata documented, despite ongoing speculation that a relationship blooms (Bothwell et al. 2009). Increased river use coincided with the commercial introduction of felt-soled waders, the expansion of the guided fishing industry, and an increase in the number of visiting anglers fishing the rivers of Vancou- ver Island. The analysis of these data entitled, ‘On the Boots of Fishermen: The History of Didymo Blooms on Van- couver Island, BC’ was published in Fisheries (Bothwell et al. 2009), with the statement:

Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 ….all of the evidence suggesting that recreational fishermen have played a role in the movement of Didymo regionally and globally is circumstantial. Nevertheless, the publication was widely accepted as an important step in initiating management actions aimed at controlling the spread of aquatic invasive species. Yet, the explanation for the spatial and temporal occurrence of blooms of D. geminata as the result of human vectors was based on coincidental timing.

Fig. 3. Didymosphenia geminata as a percentage of total diatom The Didymo trilogy biovolume during an in situ solar UVR exclusion experiment in Early in the incursion of D. geminata into New Zealand, the Little Qualicum channel on Vancouver Island during 1995 (Kelly 2001). The presence or absence of UVR had no affect on the it became clear that bloom formation must involve more abundance of D. geminata relative to other diatom taxa (two-way than the simple introduction of cells into new areas. The ANOVA, p = 0.71). observation that blooms did not form in spring-fed creeks 232 Bothwell et al.

discharging into D. geminata-affected rivers on the South paper contains solutions to pieces of the puzzle and, collec- Island, in spite of repeated introduction of cells, was demon- tively, they provide the evidence that the proximate cause strated multiple times (Sutherland et al. 2007). To address of D. geminata blooms in rivers is low concentration of P. experimentally the role of environmental factors (light We outline the ‘Didymo Trilogy’ as three chapters in our intensity and nutrient concentration of N and P) leading understanding. to bloom formation, a flume apparatus was built on the bank of the D. geminata-affected Waitaki River, adjacent to the confluence with the D. geminata-free, Otiake Spring Chapter 1: phosphorus limitation (Bothwell & Kilroy Creek (Fig. 4). This facility was utilized in a collaborative 2011) research project between Environment Canada (EC) and the The summary points from this paper are: New Zealand Institute for Water and Atmospheric Research (NIWA) during 2008–2010. Results from the NIWA–EC (1) The frequency of dividing cells (FDC) is used as studies were published (Bothwell & Kilroy 2011, Kilroy & a metric for P-limited growth rates in D. gem- Bothwell 2011a, Kilroy & Bothwell 2012). We refer to inata. FDC has been used to measure aquatic these three papers as the ‘Didymo Trilogy’ because each microbial growth for decades, but its application to D. geminata was key to understanding the blooms. (2) Exposed to high concentrations of P, D. geminata cells divide rapidly for short periods, but colonies and blooms eventually dissipate. (3) Experiments conducted year-round identified a continuing high level of P-limitation in D. gemi- nata in situ while cells remained dominant in the Waitaki River. (4) FDC was the same whether or not cells were associated with colonies and we concluded that D. geminata cells do not necessarily access P from within benthic mats.

Chapter 2: environmental control of stalk length (Kilroy & Bothwell 2011a). The summary points from this paper are:

(1) When cell division rates are low, the much longer stalks characteristic of blooms are produced. Such diversion of photosynthetically fixed carbon into extracellular compounds under conditions of nutri- ent limitation is characteristic of some diatoms (Myklestad 1995). (2) Higher light conditions also result in longer stalks. Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014

Chapter 3: relation of cell growth rates and bloom formation to dissolved phosphorus concentrations (Kilroy & Bothwell 2012) The summary points from this paper are: Fig. 4. The experimental flume apparatus used during the collab- orative research project between EC and NIWA during 2008–2010 (1) Synoptic surveys of rivers on South Island, New was located on the bank of the Waitaki River, South Island, New Zealand, adjacent to the confluence with the Otiake Spring Creek. Zealand show that the distribution of D. geminata (a) The initial design in 2008 had six flumes, all initially colonized blooms can be predicted from the SRP concen- with D. geminata using Waitaki River water. Subsequently, three tration. Blooms do not form if the mean SRP of the flumes were shifted to Otiake Spring Creek water (treat- concentration over a 24-month period (monthly ment), while the other three remained as controls and continued to sampling) exceeds ∼2 ppb (Fig. 5). receive Waitaki River water (details in Bothwell & Kilroy 2011). (b) In 2009–2010, a total of 12 flumes were employed to test addi- (2) A direct positive relationship exists between ambi- tions of P or N and light intensity using shading cloth (details in ent SRP concentration in the water and D. geminata Bothwell & Kilroy 2011; Kilroy & Bothwell 2011a). FDC (Fig. 6a), whereas an inverse relationship The Didymo story 233

Fig. 5. Algal biovolume expressed as standing crop index (% cover × mat thickness in mm) at each of 31 South Island, New Zealand, river sites surveyed between January and March 2010, in terms of broad algal groups and D. geminata, with mean SRP (diamonds) shown for each river. The dashed horizontal line indicates 2 ppb SRP.

Fig. 6. Relationship between (a) FDC and mean ambient SRP and (b) FDC and standing crop index at 15 South Island river sites where D. geminata was present.

exists between FDC and D. geminata biovolume, more precisely, excessive extracellular stalk production, is measured as a standing crop index (Fig. 6b). This is low P. There is precedence for a mucopolysaccaride pro-

Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 also a likely explanation for the absence of D. gem- duction response to low P. For example, photosynthetic inata on the North Island of New Zealand (Kilroy release of structural or non-structural exudates is a common & Unwin 2011, Rost et al. 2011) where nearly all stress response by some diatoms to low nutrient conditions rivers have naturally high SRP, >2 ppb, shown to (Hoagland et al. 1993, Myklestad 1995). Moreover, the prevent bloom establishment in rivers on the South most rapid increase in diatom-specific growth rate occurs Island (Kilroy & Bothwell 2012). below 1 ppb dissolved P, so changes in dissolved P below (3) A transect across a braid in the Waitaki River just 1 ppb are highly relevant to diatom cell division (Bothwell below a spring tributary indicated that the SRP con- 1988, 1989). The unexpected conclusion is that D. gemi- centration that inhibits blooms might even be lower nata blooms do not occur in spite of P limitation, they occur (<1 ppb) than indicated in the synoptic survey of because of it! Stalk production in response to very low P South Island. may be a strategy to move cells out of the benthic bound- ary layer and into the water column where there is greater delivery of growth-limiting P. We propose that P concen- Our epiphany trations in relatively unaffected rivers around the world are The publications that we refer to as the ‘Didymo Trilogy’ declining and D. geminata blooms are actually the result of made clear to us that the proximate cause of blooms or, that decline, not primarily the result of recent introduction. 234 Bothwell et al.

At this point, it is important to highlight the difference between blooms of D. geminata and geographic distribution of this species. New Zealand is the best example of an introduction of D. geminata (Kilroy & Unwin 2011). How- ever, while the presence of cells is obviously prerequisite, introduction alone is not the cause of bloom formation.

The ultimate causes of D. geminata blooms With low SRP identified as the proximate cause of D. gem- inata blooms, we propose four mechanisms operating at global or regional scales that could potentially result in a decline of P, i.e., oligotrophication, entering fluvial systems. We outline the following as hypotheses of the potential ultimate causes of D. geminata blooms: (1) atmospheric deposition of reactive nitrogen resulting from the burn- ing of fossil fuels and urbanization; (2) climate-induced shifts in the timing of snowmelt and growing season that decreases P inputs to rivers; (3) N-enrichment of landscapes Fig. 7. The relationship between the frequency of occurrence of during agricultural and silvicultural activities that result in D. geminata cells and total phosphorus concentration. Data from greater retention of terrestrial P; and (4) a decline in marine- the EPA Environmental Monitoring and Assessment Programme derived nutrients, particularly P, resulting from widespread (EMAP), 2000–2003. Taken from Spaulding & Elwell (2007). depletion in spawning salmon. Although these processes do not apply to all regions, they are not mutually exclusive regions (Wyatt et al. 2008). Low dissolved P as the prox- and could act synergistically. These processes are in need imate cause of D. geminata bloom formation provides a of further investigation for their role in driving blooms of parsimonious explanation for D. geminata blooms across D. geminata. spatial scales. The above potential ultimate drivers for the formation As we wrote elsewhere, ‘Didymosphenia geminata of D. geminata blooms are consistent with the world- blooms end when cell division rates are not limited by P, wide occurrence of blooms. In the case of Vancouver and blooms do not begin unless these rates are P-limited’ Island, it is now known that the onset of D. geminata (Bothwell et al. 2012). Much of the focus on D. geminata blooms in the early 1990s followed the commence- has been on identifying favourable potential-habitat condi- ment of an island-wide annual urea-N fertilization sil- tions, not on what causes bloom formation. Once the suite of vicultural programme that was among the largest of physical (higher light, low turbidity, stable substratum and its kind in North America (British Columbia Ministry flow) and chemical (specific pH range, minimum Ca and of Forests, Lands, and Natural Resource Operations; Si, maximum Na and Cl) prerequisites are met, we have http://www.for.gov.bc.ca/hfp/publications/00001/2–2-silv shown that it is the concentration of soluble available P that -stand-index.htm). Increased N inputs to landscapes will explains the timing and spatial distribution of blooms where likely lead to increased P assimilation, reducing its avail- D. geminata cells are present. ability for run-off into streams. A detailed discussion of Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 these processes is presented elsewhere. In addition to the large-scale processes we outline as Why was low P overlooked? the ultimate drivers of oligotrophication, understanding that Parameters associated with the presence of D. geminata low SRP is the proximate cause of bloom formation, affords were outlined for the United States (Spaulding & Elwell new interpretations of how local-scale factors, which poten- 2007). Using data from the EPA Environmental Monitoring tially alter P concentration, can explain smaller scale spatial and Assessment Programme, Spaulding & Elwell illustrated variability of blooms. For example, the well-known ten- that D. geminata is most frequently found in low-nutrient dency for D. geminata bloom formation to occur below water (Fig. 7). Why was the simplest explanation for the lakes and dam outlets (Kirkwood et al. 2009) takes on a increase in D. geminata abundance and the appearance of new significance in the light of dissolved P depletion in blooms as low P missed? A likely answer to this question lake surface waters during the summer. Likewise, varia- is that aquatic biologists typically associate higher algal tions in D. geminata bloom formation along river channels biomass with increases in nutrients, not decreases. have been shown to follow regions of upwelling and down- However, Eugene F. Stoermer, voiced the possibility of welling exchange with the hyporheic zone, with blooms low phosphorus. In 1994, he was contacted by the Didymo- being absent in zones of upwelling, nutrient-rich, hyporheic sphenia ad hoc group in British Columbia. His response to water, but forming in potentially P-depleted downwelling their query was prescient, indicating that he thought that the The Didymo story 235

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